RESEARCH ARTICLE

Analysis of some metallic elements and metalloids compositionand relationships in parasol mushroom Macrolepiota procera

Jerzy Falandysz1 & Atindra Sapkota2 & Anna Dryżałowska1 & Małgorzata Mędyk1 &Xinbin Feng2

Received: 20 September 2016 /Accepted: 27 April 2017 /Published online: 17 May 2017# The Author(s) 2017. This article is an open access publication

Abstract The aim of the study was to characterise the multi-elemental composition and associations between a group of 32elements and 16 rare earth elements collected by myceliumfrom growing substrates and accumulated in fruiting bodies ofMacrolepiota procera from 16 sites from the lowland areas ofPoland. The elements were quantified by inductively coupledplasma quadrupole mass spectrometry using validated meth-od. The correlation matrix obtained from a possible 48 × 16data matrix has been used to examine if any association exitsbetween 48 elements in mushrooms foraged from 16 samplinglocalizations by multivariate approach using principal compo-nent (PC) analysis. The model could explain up to 93% vari-ability by eight factors for which an eigenvalue value was ≥1.Absolute values of the correlation coefficient were above 0.72(significance at p < 0.05) for 43 elements. From a point ofview by consumer, the absolute content of Cd, Hg, Pb in capsof M. procera collected from background (unpolluted) areascould be considered elevated while sporadic/occasional inges-tion of this mushroom is considered safe. The multivariatefunctional analysis revealed on associated accumulation ofmany elements in this mushroom.M. procera seem to possesssome features of a bio-indicative species for anthropogenic Pbbut also for some geogenic metals.

Keywords Foraging . Fungi . Heavymetals . Traceelements .Mushrooms . Poland

Introduction

Macrolepiota procera (Scop.) Sing., commonly known asField Parasol, Parasol Mushroom or Shaggy Parasol, is asaprobe. It is edible and widely collected in temperate regionsand sub-tropical regions such as India, Thailand, China orPakistan and across Europe (Kułdo et al. 2014; Melgar et al.2016; Stefanović et al. 2016a; Širić et al. 2016; Xiaolan 2009).The pileus of M. procera are highly valued by locals. This isbecause of the taste and aroma of the cooked fresh individ-uals—sautéed, roasted, fried in butter or grilled, roasted witheggs or stuffed and broiled. According to some cooking rec-ipes, the dried caps of M. procera could be resoaked in freshwater and both; the flesh and macerate (liquid) can be used fora dish. Frying ofM. procerawith butter or vegetable oil can tosome degree result in leakage of elements out of a fleshy capas was observed for fried Cantharellus cibarius and Boletusedulis and radiocaesium (137Cs) (Steinhauser and Steinhauser2016). Nevertheless, caps of M. procera before frying areusually surrounded in flour, then in a drooping egg. Hence,any serious leakage of bio- or toxic elements out of a cap (orprepared dish) seems unlikely. Re-soaking of dried caps ofM. procera in fresh water can have a more pronounced influ-ence on possible leakage out of minerals but no figures areavailable. Blanching (parboiling) can decrease content of min-erals in cooked mushrooms and also pickling, while a fate of aparticular element can be different and highly dependent on itschemical form, localization within cells and type of chemicalbonds made (Drewnowska et al. 2017a, 2017b; Falandysz andDrewnowska 2017).

Responsible editor: Philippe Garrigues

* Jerzy Falandyszjerzy.falandysz@ug.edu.pl

1 Laboratory of Environmental Chemistry & Ecotoxicology, GdańskUniversity, 63 Wita Stwosza Str, 80-308 Gdańsk, Poland

2 State Key Laboratory of Environmental Geochemistry, Institute ofGeochemistry, Chinese Academy of Sciences, Guiyang 550002,China

Environ Sci Pollut Res (2017) 24:15528–15537DOI 10.1007/s11356-017-9136-9

http://orcid.org/0000-0003-2547-2496http://crossmark.crossref.org/dialog/?doi=10.1007/s11356-017-9136-9&domain=pdf

M. procera prefers lighted and warm places. Especially incalcareous and sandy soils that are well-drained in forests,meadows and gardens (Rizal et al. 2015). In Asia,Macrolepiota species such as M. procera, M. dolichaula(Berk. & Broome) Pegler & R.W. Rayner, M. gracilenta(Krombh.) Wasser are consumed by locals (Woźniak 2009).In Europe, M. procera is mistaken with the deadly Amanitaphalloides (Vaill. ex Fr.) Link., (Death Cap, or DestroyingAngel) and Chlorophyllum molybdites (G. Mey.) Massee(False Parasol). Because of its popularity and versatility, it isalso cultivated in kitchen gardens. This mushroom, like cer-tain other macromycetes, when found in its natural habitats inbackground (unpolluted) areas, is efficient in accumulatingtoxic mercury (Hg), cadmium (Cd), lead (Pb), silver (Ag)and some micronutrients in fruiting bodies (Falandysz et al.2001, 2003; García et al. 2009; Krasińska and Falandysz,2016; Gąsecka et al. 2017; Melgar et al. 2009, 2016; Mędyket al. 2017; Mleczek et al. 2013, 2016a, b, 2017; Saba et al.2016a, b, c; Sar ikurkcu et al . 2015). Due to i tsbioaccumulating property, many researchers are continuouslyinvestigating Macrolepiota species commonly collected bylocals for their essential microminerals, macrominerals, met-alloids and toxic metals contents in the fruiting bodies(Baptista et al. 2009; Falandysz et al. 2007a; Gucia et al.2012a, b; Řanda et al. 2005).

This study attempts to investigate fruiting bodies ofM. procera for its co-occurrence and associations betweenmetallic elements and metalloids such as Ag, As, Ba, Be, Bi,Cd, Co, Cs, Cu, Ga, Ge, Hf, Hg, In, Li, Mo, Nb, Ni, Pb, Rb,Sb, Sn, Sr, Ta, Th, Ti, Tl, U, V, W, Zn, Zr and rare earthelements (Sc, Y, La, Ce, Pr, Nd, Sm, Eu, Gd, Tb, Dy, Ho,Er, Tm, Yb and Lu) accumulated in caps and stipes.

Materials and methods

Fruiting bodies ofM. procerawere collected from 16 differentsites from the lowland areas in northern and central regions ofPoland: Włocławek - outskirts (forests) (52° 39′ 33″N 19° 04′05″ E) [site 1; Fig. 1]; Pomerania, Lębork (54° 33′ N 17° 45′E) [site 2]; Warmia land, Olsztyn/Szczytno (53° 47′ N 20° 30′E/53° 33′ 46″ N 20° 59′ 7″ E) [3]; Trójmiejski LandscapePark—Gdańsk-Wrzeszcz (54° 22′ 10.1″ N 18° 35′ 47.0″ E)[site 4]; Augustów Primeval Forest (53° 87′ 28″ 0 N 22° 97′43″ 0 E) [site 5]; Tuchola Pinewoods, Łuby (53° 42′ 30″N 18°22′ 53″ E) [6]; Wdzydze Landscape Park (54° 00′ 47″ N 17°54′ 04″ E) [7]; Warmia land, Sarnówek (53° 39′ 33.78″ N 19°35′ 16.83″ E) [site 8]; Toruń—outskirts (forests) (53° 01′ 20″N 18° 36′ 40″ E) [site 9]; Vistula River Sand-bar, Stegna (54°19′ 35″ N 19° 6′ 44″ E) [10]; Nadwarciańska Forest (52° 12′00″ N 17° 54′ 00″ E) [site 11]; Warmia land, Jeziorak lake—island of Gierszak (53° 43′ 23.24″ N 19° 36′ 46.80″ E) [site12]; Zielonka near Poznań forests (52° 33′ 13″ N 17° 06′ 49″

E) [site 13]; Tuchola Pinewoods, Osie (53° 35′ 57″ N 18° 20′41″ E) [site 14]; Kukawy/Goreń region (52° 33′ 52″N 19° 11′42″ E/52° 31′ 50″ N 19° 17′ 22″ E) [site 15] and Bydgoszczforests (53° 7′ N 18° 0′ E) [site 16] (Fig. 1, Table 1). The sitesof M. procera collection can be considered as background(unpolluted) and without local or regional major emitters ofheavy metals in forests of the lowland Poland. A major branchof metallurgy and ore mining industry is localized in the cen-tral (iron mill near Warszawa, Fig. 1) and southern regions ofPoland (Brzezicha-Cirocka et al. 2016).

Soils at the forested areas of the lowland Poland are pod-zolic soils which were formed by pine and mixed/pine forestsand of mesophilic deciduous and coniferous forests in thezone of warm-temperate climate and are slightly acidic(Degórski 2004). Typical soils there are podzols,pseudopodzols and rusty soils poor in nutrients and developedfrom fluvioglacial sands with a texture of sands and some-where in the outskirts of lakes and rivers with peats, peat-muck soils and vertisols. The tree covers are dominated byneedle trees such as Pinus sylvestris L. and in lower propor-tion with Picea abies (L.) H. Karst., Larix decidua Mill.,Betula pendulaRoth, Betula pubescensEhrh.,Alnus glutinosa(L.) Gaertn., Quercus robur L., Quercus petraea, (Matt.)Liebl., Fagus sylvatica L. (Statistical Office 2014). Each com-posite sample of caps and whole fruiting bodies consisted of10 to 30 individuals.

Fig. 1 Sampling sites of M. procera (site 1: Włocławek—outskirts(forests), site 2: Pomerania, Lębork; site 3: Warmia land, Olsztyn/Szczytno; site 4: Trójmiejski Landscape Park—Gdańsk-Wrzeszcz; site5: Augustów Primeval Forest; site 6: Tuchola Pinewoods, Łuby; site 7:Wdzydze Landscape Park; site 8: Warmia land, Sarnówek; site 9:Toruń—outskirts (forests); site 10: Vistula River Sand-bar, Stegna; site11: Nadwarciańska Forest; site 12: Warmia land, Jeziorak lake—island ofGierszak; site 13: Zielonka near Poznań forests; site 14: TucholaPinewoods, Osie; site 15: Kukawy/Goreń region and site 16:Bydgoszcz forests; see also Table 1)

Environ Sci Pollut Res (2017) 24:15528–15537 15529

Tab

le1

Elementsin

fruitin

gbodies

ofM.procera

(mgkg

−1drybiom

ass)

Place,year,num

berof

specim

ensandmorphologicalpart*

Ag

As

Ba

Be

Bi

Cd

Co

Cs

Cu

Ga

Ge

Hf

Hg

InLi

Mo

AugustówPrimevalForest,2001

(n=15;c)[5]a

1.9

0.93

5.4

0.019

0.0046

9.4

0.23

0.097

830.18

0.033

0.050

2.8

0.0011

0.23

0.45

Pom

erania,L

ębork,2003

(n=30;c)ltl

[2]

1.4

0.69

1.7

0.0080

0.0021

2.4

0.31

0.034

130

0.12

0.022

0.022

2.5

0.0047

0.038

0.42

TLP,2001

(n=23;c)a[4]

0.86

0.47

2.5

0.0083

0.0058

0.75

0.084

0.039

570,13

0,025

0.020

1.9

0.0018

0.73

0.37

VistulaRiver

Sand-bar,S

tegna,2003

(n=10;c)[10]

0.98

0.43

100.021

0.0065

4.3

0.092

0.051

990.16

0.027

0.025

2.0

0.0023

0.48

0.49

WLP,1994/2001(n

=21;c)[7]

1.0

0.61

4.4

0.021

0.0064

1.8

0.18

0.041

960.18

0.040

0.049

1.1

0.0021

1.0

0.44

Warmialand,G

ierszak,(n

=15;c)[12]

0.72

0.64

3.1

0.015

0.031

1.1

0.13

0.022

750.14

0.028

0.034

2.0

0.0029

0.094

0.39

Warmialand,S

arnówek,2001(n

=11;c)[8]

0.65

0.37

2.0

0.0056

0.0010

0.65

0.056

0.013

830.12

0.022

0.021

1.5

0.0017

0.49

0.35

Olsztyn/Szczytno,2002

(n=25;c)[3]

0.94

0.86

0.85

0.0086

0.0067

1.7

0.24

0.030

820.097

0.014

0.0045

1.9

0.0030

0.019

0.44

TucholaPinew

oods,Ł

uby,1995

(n=15;c)[6]

2.5

1.3

3.3

0.013

0.0041

2.2

0.16

0.036

100

0.14

0.030

0.022

2.0

0.0027

2.7

0.42

Włocław

ek—outskirts(forests),2004

(n=15;c)[1]

4.1

1.0

3.7

0.021

0.0035

0.52

0.070

0.032

800.15

0.048

0.029

1.8

0.0052

0.074

0.72

Toruń—

outskirts(forests),(n

=15;c)[9]

0.83

0.49

4.0

0.013

0.0019

1.3

0.062

0.045

810.15

0.036

0.018

2.8

0.0027

2.0

0.44

NadwarciańskaForest,1999

(n=15;c)[11]

1.2

0.56

0.85

0.0088

0.0044

0.84

0.034

0.036

830.083

0.014

0.0032

2.2

0.0039

0.012

0.34

Zielonkanear

Poznań,2001(n

=15;c)[13]

7.9

5.4

2.5

0.023

0.0034

0.73

0.053

0.028

100

0.14

0.057

0.019

1.1

0.0035

0.094

1.4

Mean

1.9

1.1

3.9

0.014

0.0063

2.1

0.13

0.039

880.14

0.030

0.024

2.0

0.0029

0.62

0.61

SD2.0

1.3

2.4

0.006

0.0073

2.4

0.09

0.020

170.03

0.012

0.014

0.5

0.0012

0.85

0.28

TucholaPinew

oods,O

sie,2000

(n=15;w

)[14]

1.9

0.54

5.3

0.020

0.067

1.9

0.12

0.029

110

0.17

0.038

0.032

1.6

0.0036

0.90

0.38

Kukaw

y/Goreń

region,2001(n

=15;w

)[15]

1.1

0.66

2.2

0.0045

0.0043

1.1

0.13

0.041

110

0.11

0.024

0.015

1.4

0.0043

0.35

0.37

Bydgoszcz

-outskrits,2001(n

=15;w

)[16]

2.0

0.49

5.6

0.020

0.0047

1.0

0.18

0.037

930.19

0.043

0.030

1.3

0.0019

0.70

0.38

Mean

1.3

0.56

4.4

0.015

0.025

1.3

0.14

0.036

100

0.16

0.038

0.026

1.4

0.0033

0.65

0.38

SD0.5

0.09

1.9

0.009

0.036

0.3

0.03

0.006

90.04

0.010

0.009

0.1

0,0012

0.28

0.01

Place,year,num

berof

specim

ensandmorphologicalpart*

Nb

Ni

Pb

Rb

SbSn

Sr

TaTh

Ti

Tl

UV

WZn

Zr

AugustówPrimevalForest,2001

(n=15;c)[5]

0.058

0.42

6.1

500.057

0.054

1.4

0.018

0.040

320.063

0.014

1.0

0.012

632.1

Pom

erania,L

ębork,2003

(n=30;c)[2]

0.027

0.38

1.6

570.012

0.096

0.49

0.013

0.012

220.031

0.0057

1.3

0.015

651.2

TLP,2001

(n=23;c)[4]

0.047

0.21

2.2

580.011

0.25

0.73

0.015

0.022

270.024

0.0081

1.1

0.019

570.75

VistulaRiver

Sand-bar,S

tegna,2003

(n=10;c)[10]

0.058

0.39

4.6

380.020

0.18

1.4

0.016

0.035

390.021

0.016

1.1

0.017

691.2

WLP,1994/2001(n

=21;c)[7]

0.090

0.33

3.7

400.013

0.27

1.1

0.026

0.051

460.036

0.016

1.5

0.025

672.1

Warmialand,G

ierszak,(n

=15;c)[12]

0.069

0.22

2.0

360.0095

0.28

0.87

0.010

0.017

330.023

0.010

1.3

0.019

541.4

Warmialand,S

arnówek,2001(n

=11;c)[8]

0.055

0.12

0.92

6.2

0.0068

0.14

0.70

0.015

0.023

270.0073

0.0071

1.1

0.017

600.93

Olsztyn/Szczytno,2002

(n=25;c)[3]

0.014

0.22

1.4

470.0075

0.19

0.26

0.012

0.0081

150.043

0.0027

0.84

0.018

540.17

TucholaPinew

oods,Ł

uby,1995

(n=15;c)[6]

0.063

0.56

3.5

250.016

0.24

0.76

0.018

0.037

260.026

0.013

1.1

0.024

560.89

Włocław

ek-outskirts,2004

(n=15;c)[1]

0.068

0.26

2.8

200.026

0.13

1.3

0.017

0.023

340.013

0.010

1.6

0.040

921.3

Toruń-outskirts,(n

=15;c)[9]

0.061

0.18

3.3

340.012

0.17

1.1

0.021

0.025

290.045

0.010

1.2

0.025

580.83

NadwarciańskaForest,1999

(n=15;c)[11]

0.009

0.53

2.0

150.0035

0.22

0.43

0.014

0.0043

130.0075

0.0019

1.1

0.0089

580.13

Zielonkanear

Poznań,2001(n

=15;c)[13]

0.042

0.26

2.8

100.021

0.30

0.94

0.0086

0.025

290.0066

0.010

3.3

0.038

150

0.91

Mean

0.051

0.31

2.8

330.017

0.19

0.88

0.016

0.029

290.027

0.0091

1.3

0.021

691.1

SD0.023

0.01

1.4

170.014

0.07

0.37

0.005

0.013

90.017

0.0045

0.6

0.009

260.6

15530 Environ Sci Pollut Res (2017) 24:15528–15537

The fungal biomass dehydrated and grounded into a finepowder before analysis was dried at a temperature of 65 °C for12 h and a subsample (about 200-mg samples made in dupli-cate) was mixed with 3 mL solution of ultrapure concentratednitric acid (HNO3, 65%,) and 1 mL of ultrapure hydrofluoricacid (HF) in a polytetrafluoroethylene tubes (PTFE). Then, thetubes were screw tightened in stainless steel jackets and placedin an oven at 150 °C for 78 h. The solutions obtained wereevaporated to dryness at 110 °C, to remove the excess of HF(Bi et al. 2007). Then, it was dissolved in 1 mL of HNO3 tomake the final volume up to 50 mL, which was then trans-ferred to a sample tube. As an internal standard, rhodium (Rh)(10–20μg/L) was added to the samples prior to the QuadrupleICM-MS analysis (The Quadrupole-ICP-MS ELAN DRC-e;PerkinElmer, Waltham, MA, USA). In order to achieve goodanalytical quality control, quality assurance and blanks of cer-tain certified reference materials were examined. Each ele-ment was measured three times and the values of relativestandard deviation (RSD) were within 5% in the samplesand the certified values for certified reference materials(CRM) (Liang and Grégoire 2000). The CRMs used werecitrus leafs (GBW 10020) and soil (GBW 07405) producedby the Institute of Geophysical and Geochemical Exploration,China (Shi et al. 2011).

The computer software Statistica, version 10.0 (StatsoftPolska, Kraków, Poland), was used for statistical analysis ofdata and for graphical presentation of the results of two di-mensional multiple scatter plot relationships between thevariables.

Results and discussion

Toxic metallic elements and metalloids

Cadmium (Cd), mercury (Hg) and lead (Pb) are common con-stituents of M. procera and they occurred in caps at2.1 ± 2.4 mg kg−1 db (arithmetic mean plus standard devia-tion) (Cd), 2.0 ± 0.5 mg kg−1 db (Hg) and 2.8 ± 1.4 mg kg−1 db(Pb) (Table 1). If assume that Cd, Hg and Pb remain in theflesh of caps, when they are sautéed, roasted, fried in butter,grilled or roasted with eggs, a single mushroom dish (100 to300 g) certainly will provide an elevated quantity of eachheavy metal (0.021–0.063 mg of Cd per capita, 0.02–0.06 mg Hg per capita and 0.028–0.084 mg Pb per capita).Hence, frequent eating of caps of M. procera could be notrecommended. Nevertheless, unknown is the bioaccessibilityof Cd, Pb and Hg contained in caps ofM. procera for humans.

Contamination with toxic Cd and Pb of edible mushroomsis regulated in the European Union but not in the case of Hg,As or any other inorganic contaminant. The maximum limit ofCd established is 0.2 mg kg−1 fresh product (2.0 mg kg−1 indried product—assuming moisture content is at 90%) inTa

ble1

(contin

ued)

TucholaPinew

oods,O

sie,2000

(n=15;w

)[14]

0.087

0.25

2.7

160.016

0.091

1.5

0.019

0.035

440.021

0.013

1.8

0.021

641.6

Kukaw

y/Goreń

region,2001(n

=15;w

)[15]

0.027

0.28

2.2

420.017

0.076

0.86

0.019

0.012

250.034

0.0058

1.6

0.016

640.70

Bydgoszcz

-outskrits,2001(n

=15;w

)[16]

0.085

0.35

2.0

190.019

0.21

1.9

0.017

0.052

330.030

0.019

1.1

0.025

511.3

Mean

0.066

0.29

2.3

260.017

0.13

1.4

0.018

0.033

340.028

0.013

1.5

0.021

601.2

SD0.034

0.05

0.4

140.001

0.07

0.5

0.001

0.020

90.007

0.007

0.4

0.004

70.5

*c,s,w

(caps,stipes,w

holefruitingbodies,respectively);T

LPTrójm

iejski

Landscape

Park—Gdańsk-Wrzeszcz;WLP

Wdzydze

Landscape

Park

aLocalizationof

thesamplingsite(see

Fig.1

)

Environ Sci Pollut Res (2017) 24:15528–15537 15531

farmed Agaricus bisporus (J.E.Lange) Imbach, Pleurotusostreatus (Jacq.) P. Kumm. and Lentinula edodes (Berk.)Pegler. This limit for Cd is 1.0 mg kg−1 fresh product(10 mg kg−1 in dried product) for other fungi (EC, 2006,2008). In the case of Pb and cultivated mushroomsmentioned,the maximum allowed limit is 0.3 mg kg−1 fresh product(3.0 mg kg dried product) (EC, 2006, 2008). M. procera inthis study showed at the average on little contamination with

Cd, i.e., in caps, concentration levels were well below10 mg kg−1 dried product (Table 1). An exception were indi-viduals collected from the Augustowska Primeval Forest sitewhich contained Cd in caps at 9.4 mg kg−1 dry biomass(Table 1). The Augustowska Primeval Forest region is consid-ered as pristine (green lungs) and localized faraway of majoremitters of heavy metals. A possible explanation for elevatedconcentration level of Cd in mushrooms can be because of a

Table 2 Factor loadings (Varimax normalized)

Eigenvalues 24.25 7.26 4.06 2.31 2.14 2.10 1.40 1.05Total variance (%) 50.52 15.13 8.46 4.82 4.47 4.37 2.91 2.18Cumulative % 50.52 65.65 74.11 78.94 83.40 87.77 90.68 92.86Variables PC1 PC2 PC3 PC4 PC5 PC6 PC7 PC8

Li 0.24 −0.16 −0.08 0.23 0.28 0.72 −0.12 0.09Be 0.76 0.52 0,08 0.12 0.11 −0.08 0.00 −0.07Sc 0.58 −0.08 0.18 0.08 0.25 −0.65 −0.07 0.00V 0.01 0.93 −0.07 −0.09 −0.06 −0.01 −0.05 −0.24Co 0.04 −0.20 0.23 −0.15 0.19 0.03 0.84 −0.11Ni 0.02 −0.05 0.32 −0.07 0.79 0.19 −0.04 0.02Cu 0.08 0.15 −0.07 −0.58 0.52 0.15 0.24 −0.37Zn −0.01 0.95 0.00 −0.05 0.05 −0.16 −0.12 0.03Ga 0.94 0.13 0.22 0.10 −0.04 0.06 0.12 −0.03Ge 0.63 0.74 −0.01 0.01 −0.11 0.10 −0.03 0.13As −0.15 0.95 0.05 0.16 0.12 −0.03 −0.06 −0.07Rb −0.11 −0.36 0.33 0.05 0.07 −0.19 0.70 0.23Sr 0.92 0.08 0.14 −0.11 −0.07 −0.03 −0.19 -0.02Y 0.97 -0.05 0.17 −0.03 0.03 −0.10 −0.06 0.03Zr 0.80 0.10 0.23 0.01 −0.10 0.02 0.37 −0.18Nb 0.92 0.02 −0.18 0.17 −0.12 0.18 0.03 −0.10Mo −0.02 0.96 0.00 0.06 0.06 −0.15 −0.08 0.09Ag 0.06 0.97 0.00 −0.06 0.10 −0.01 −0.12 0.05Cd 0.29 −0.12 0.87 0.01 0.18 −0.15 0.19 −0.10In −0.30 0.35 −0.12 −0.77 0.07 −0.10 0.11 0.04Sn −0.05 0.35 −0.13 0.86 0.10 0.05 0.06 0.08Sb 0.44 0.24 0.81 −0.13 −0.06 −0.06 0.11 0.07Cs 0.26 −0.08 0.93 0.00 0.08 0.01 0.13 0.13Ba 0.80 −0.13 0.20 0.02 0.31 −0.27 −0.19 0.04La 0.92 −0.01 0.26 −0.04 0.00 0.21 0.08 −0.15Ce 0.92 −0.03 0.19 −0.02 0.01 0.25 0.09 −0.19Pr 0.92 −0.03 0.22 −0.03 0.01 0.23 0.04 −0.18Nd 0.94 −0.04 0.15 0.03 0.06 0.22 0.01 −0.15Sm 0.97 −0.10 0.10 0.05 0.02 0.16 0.03 −0.07Eu 0.93 0.15 0.12 −0.07 −0.15 0.11 −0.01 −0.12Gd 0.95 −0.12 0.19 0.04 0.09 0.15 0.04 −0.01Tb 0.96 −0.07 0.19 0.03 0.06 −0.02 0.00 −0.02Dy 0.95 −0.08 0.22 0.06 0.09 −0.03 −0.10 0.01Ho 0.97 −0.03 0.14 −0.05 0.00 −0.10 −0.06 0.05Er 0.98 0.03 0.08 −0.04 −0.01 −0.11 −0.05 0.09Tm 0.93 0.25 0.08 −0.05 −0.03 −0.17 −0.01 0.11Yb 0.97 0.06 0.07 −0.10 −0.07 −0.13 −0.04 0.08Lu 0.96 0.11 −0.01 −0.05 −0.06 −0.09 0.01 0.20Hf 0.78 0.06 0.27 0.12 −0.12 0.03 0.37 −0.13Ta 0.50 −0.33 0.19 −0.11 −0.06 0.62 0.04 0.08W 0.37 0.77 −0.12 −0.03 −0.24 0.19 0.05 0.32Tl 0.15 −0.28 0.66 0.04 −0.12 0.20 0.52 0.07Pb 0.51 0.12 0.73 0.10 0.27 0.02 −0.01 0.09Bi 0.33 −0.07 −0.19 −0.12 −0.13 −0.12 −0.03 −0.76Th 0.87 0.05 0.13 0.25 0.13 0.30 0.05 -0.01U 0.93 0.07 0.08 0.21 0.20 0.07 0.00 0.00Ti 0.90 0.09 −0.07 0.05 −0.07 −0.01 0.08 −0.21Hg −0.06 0.16 −0.02 0.06 0.89 −0.13 0.18 0.13

In italics are the significant loadings used for each principal component

15532 Environ Sci Pollut Res (2017) 24:15528–15537

specific geochemistry of a soil parent material there, but thiswas not studied.

M. procera from the five sites contained Pb in caps atconcentration level in the range of 3.3–6.1 mg kg−1 dry prod-uct (Table 1), which exceeded a limit set for farmed mush-rooms mentioned earlier. Maximum contamination with Pbwas similar to Cd in mushrooms from the AugustowskaPrimaeval Forest.

Also, silver (Ag) occurred in caps ofM. procera at contentcomparable to what was observed for Cd, Hg, Pb, i.e., at1.9 ± 2.0 mg kg−1 db. An intake of Ag per capita could besimilar as is for Cd, Hg and Pb. Silver, like Cd, Hg and otherchalcophile elements, has affinity to sulphur. The elements Ag,Cd and Hg are well bio-concentrated by M. procera and sev-eral other mushrooms (Chudzyński et al. 2011; Falandysz et al.1994; Stefanović et al. 2016a, 2016b). Arsenic (As) was incaps at 1.1 ± 1.3 mg kg−1 db (Table 1), which was at relativelylow concentration level while compounds of As were not stud-ied. The inorganic compounds of As are most toxic whilemuch less or almost non-toxic are considered organic arseniccompounds—they can be found in various (species-specific)proportion in mushrooms but can be well accumulated by fun-gi from a soil polluted with As (Falandysz and Rizal 2016;Falandysz et al. 2017a). There is no other data available onAs in M. procera from background areas of Poland.

Available data on antimony (Sb) and thallium (Tl) inM. procera are scarce (Falandysz et al. 2001). In this study,Sb was in caps ofM. procera at 0.017 ± 0.014 mg kg−1 db andTl at 0.027 ± 0.017 mg kg−1 db, which are negligible quanti-ties if compared to other toxic chalcophile elements men-tioned earlier. In a view of the human consumer, there is adeficit of information on a possible absorption rate of a par-ticular metallic elements and metalloids contained in cookedcaps of this mushroom, when ingested. For example, the bio-availability of Cd from the blanched or pickled mushroomCantharellus cibarius is considered to be not greater than20% (unpublished, JF).

Other elements determined can be considered largely asnatural compounds absorbed from the geochemical back-ground that occurred at typical but not elevated concentrationlevels in M. procera. For example, the chalcophile elementsdetermined such as gallium (Ga), germanium (Ge), indium(In), tin (Sn) and bismuth (Bi) were at the small contents incaps. They contained them (in mg kg−1 db), respectively, at0.14 ± 0.03 (Ga), 0.030 ± 0.012 (Ge), 0.0029 ± 0.0012 (In),0.19 ± 0.07 (Sn) and 0.0063 ± 0.0076 (Bi). A chalcophilecopper (Cu) and zinc (Zn) were both the major trace elementsin caps, which contained Cu at 88 ± 17 mg kg−1 db and Zn at69 ± 26 mg kg−1 db (Table 1). Copper and zinc tend to

Fig. 2 Principal component analysis of the trace metallic elements,metalloids and rare earth elements associations in M. proceramushroom (a–c) in the panorama of the Varimax normalized matrices

Environ Sci Pollut Res (2017) 24:15528–15537 15533

accumulate similarly in the hymenophore and the rest of thefruiting body of M. procera (Alonso et al. 2003). Regardlessof the contents of toxic elements such as Cd, Pb and Hg, thecaps of M. procera seem a good source of Cu and Zn.

The alkali metals such as lithium (Li), rubidium (Rb) andcaesium (Cs) were in caps at 0.62 ± 0.85 mg kg−1 db (Li),33 ± 17 mg kg−1 db (Rb) and 0.039 ± 0.020 mg kg−1 db (Cs).For lithium there was a wide span of values for the sites andrange from 0.012 to 2.7 mg kg−1 db (Table 1). There is noother data published on the element Li in M. procera to con-firm observation from this study. Both Rb and Cs (stable133Cs) were at a small content in M. procera, while muchricher in both elements are mycorrhizal mushrooms(Falandysz and Borovička 2013). A low status of stable133Cs (and also Rb) in fruiting bodies of M. procera, whenrelated to certain other mushrooms, seem to explain a lowsusceptibility of this mushroom for contamination with radio-active caesium (134/137Cs).

The alkali earth metals such as beryllium (Be), strontium(Sr) and barium (Ba) highly differed in their content inM. procera . The element Be occurred in caps at0.014 ± 0.006 mg kg−1 db, the Sr was at 0.88 ± 0.37 mg kg−1

db and the Ba was at 3.9 ± 2.4 mg kg−1 db. Data on Ba inM. procera provided in this study (Table 1) showed on a greatercontent, when compared to results for M. procera obtained byargon plasma atomic emission spectroscopy (Ouzouni andRiganakos 2007).

Other elements for which are available a few sets of data ontheir occurrence and accumulation by fungi in fruiting bodiesare cobalt (Co), nickel (Ni), thorium (Th), titanium (Ti), ura-nium (U) and vanadium (V) (Aloupi et al. 2011; Baumannet al. 2014; Borovicka et al. 2011; Falandysz et al. 2007b;Vetter and Siller 1997;Řanda et al. 2005). Amongmushroomsthat were studied so far, the Fly Agaric Amanita muscaria (L.)Lam. was identified as the specific accumulator of vanadium,while not one specifically efficiently accumulated Co, Ni, Th,Ti or U. The caps of M. procera contained Co at0.13 ± 0.09 mg kg−1 db, Ni at 0.31 ± 0.01 mg kg−1 db, Th at0.029 ± 0.013 mg kg−1 db, U at 0.0091 ± 0.0045 mg kg−1 db,Ti at 29 ± 9 mg kg−1 db, and V at 1.3 ± 0.6 mg kg−1 db.

The obtained results for elements such as hafnium (Hf),which occurred in caps at 0.024 ± 0.014 mg kg−1 db, tantalum(Ta) at 0.016 ± 0.005 mg kg−1 db and wolfram (W) at0.021 ± 0.009 mg kg−1 db. They all agree with a single resultobtained for a whole fruiting body of M. procera from theCzech Republic and obtained by neutron activation analysis(Řanda and Kučera 2004).

Fig. 3 Principal component analysis of the trace metallic elements,metalloids and rare earth elements associations in its samplinglocalizations (a–c) of M. procera in the panorama of the Varimaxnormalized matrices

15534 Environ Sci Pollut Res (2017) 24:15528–15537

Absent in the available literature are data on occurrence inM. procera of the metallic elements such as molybdenum(Mo), niobium (Nb) and zirconium (Zr). Those elements oc-curred in caps at 0.61 ± 0.28 mg kg−1 db (Mo),0.051 ± 0.023 mg kg−1 db (Nb) and 1.1 ± 0.6 mg kg−1 db(Zr) (Table 1).

Multivariate analysis of data

A possible relationship between 48 metallic elements (includ-ing data on rare earth elements) (Falandysz et al. 2017b) andmetalloids accumulated in caps and whole fruiting bodies byfungus M. procera collected at 16 spatially distributed placesin the northern and central regions of Poland has been exam-ined using the principal component (PC) analysis(Wyrzykowska et al. 2001). In this multivariate approach,the results from examination of possible 48 × 16 data matrixare summarised in Table 2 (results for 48 × 13 data matrixobtained separately for caps are not shown). This was possibleto explain up to 93% variability in the 48 × 16 data matrix byeight factors as well as up to 96% variability in the 48 × 13data matrix by eight factors for which an eigenvalue value was≥1. Absolute values of the correlation coefficient were above0.72 (significance at p < 0.05) for 43 elements in the 48 × 16data matrix and above 0.70 for 42 elements in the 48 × 13 datamatrix.

The PC1 was under influence by variables associatedwith positively correlated Ba, Be, Ce, Dy, Er, Eu, Ga, Gd,Hf, Ho, La, Lu, Nb, Nd, Pr, Sm, Sr, Tb, Th, Ti, Tm, U, Y,Yb and Zr, which are largely the lithophile elements thatare characterised by similar chemical properties—alkalineearth metals (Be, Ba, Sr), which, together with Mg and Ca,have all a somewhat similar chemical and physical prop-erties (Tabouret et al. 2010). The Be, Ba and Sr are moreor less alike to Ca in the environment and biological sys-tems and Sr can displace Ca. In the PC1 associations,positively correlated were also the rare earth elements(RREs) which are similar to Ca and all have similar chem-ical and physical properties and tend to exist together. ThePC1 was also under the influence by variables associatedwith positively correlated some other elements (Y, Zr, Nb,U, Th, Ti) and also Ga. The PC2 was under the influenceby positively correlated Ag, As, Ge, Mo, V, W and Zn, andPC 3 by variables with positively correlated Cd, Cs, Pband Sb. The PC4 was influenced by variables associatedwith negatively correlated element indium (In) and posi-tively correlated Sn, the PC5 was with positively correlat-ed Ni and Hg, the PC6 was with Li, the PC7 was with Coand the PC8 with negatively correlated Bi (Table 2). Theassociations among the elements determined and places ofmushroom collection in the factor space as a PCA arepresented graphically in Figs. 1 and 2.

M. procera as a decomposer absorbs inorganic compoundsfrom a digested decaying plant matter in soils and from thesoil solution. Hence, a significant difference in content of theparticular element in mushroom between the sampling local-ization could be largely associated with geochemistry of thesoil parent material and content of a particular element andtheir availability or co-absorption, composition of decayingplant matter and anthropogenic pollution.

The localization Trzebiesza near Poznań—no. 13 on a map(associated with PC2) was separated due to significantly ele-vated content of Ag, As, Mo, Vand Zn inM. procera (Figs 1aand Fig. 2a). Contrary, the localization Sarnówek in a forestedand agricultural region of the Warmia land—no. 8 on a map(associated with PC 3) was separated due to small content ofCd, Cs, Pb and Sb in mushrooms (Fig. 2a and Fig. 3a). Thelocalization of the Augustów Primeval Forest—no. 5 (associ-ated with PC3) was characterised by elevated content of Cd,Pb and Sb, which could be related to known a deep in theground deposits of some metal ores there. This localizationwas also associated with PC4 by small content of Sn and inmushrooms.

For the localization near Łuby in the Tuchola Pinewoods(no. 6) was strong relationship between Hg and Ni (associatedwith PC 5). The localization of Kościerzyna (no. 7) because ofLi (PC6); the localization Lębork (no. 2), because of Co (as-sociated with PC7), and the localization Island Gierszak (no.12) because of Bi (associated with PC8) (Figs 1 and 2,Table 2).

Conclusion

M. procera foraged from the background areas could becharacterised by elevated content of toxic Cd, Hg and Pb inedible caps of the fruiting bodies while less of As, which is aspecies-specific feature. Since caps of M. procera are cookedwithout blanching, which could, to some degree, reduce thecontent of As, Cd, Hg and Pb, a frequent eating of this mush-room may be not desired. Also, toxic Sb and Tl were inM. procera at small but probably typical concentrations.M. procera seem to possess some features of a bio-indicativespecies for anthropogenic Pb but also for some geogenicmetallicelements. The bio-elements Cu and Zn but also several otherelements were inM. procera in a narrow range of concentrationlevels that can be explained by a lack of major environmentalproblems with heavy metals in the regions examined.

Open Access This article is distributed under the terms of the CreativeCommons At t r ibut ion 4 .0 In te rna t ional License (h t tp : / /creativecommons.org/licenses/by/4.0/), which permits unrestricted use,distribution, and reproduction in any medium, provided you give appro-priate credit to the original author(s) and the source, provide a link to theCreative Commons license, and indicate if changes were made.

Environ Sci Pollut Res (2017) 24:15528–15537 15535

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http://dx.doi.org/10.5943/mycosphere/6/4/3http://dx.doi.org/10.5943/mycosphere/6/4/3https://www.google.pl/search?q=gatunki+drzewa+w+polsce&ie=utf-8&oe=utf-8&client=firefox-b&gfe_rd=cr&ei=GaLvWNGjIOOv8wf2g634Dw%23q=major+tree+species+in+polish+forests&start=10https://www.google.pl/search?q=gatunki+drzewa+w+polsce&ie=utf-8&oe=utf-8&client=firefox-b&gfe_rd=cr&ei=GaLvWNGjIOOv8wf2g634Dw%23q=major+tree+species+in+polish+forests&start=10https://www.google.pl/search?q=gatunki+drzewa+w+polsce&ie=utf-8&oe=utf-8&client=firefox-b&gfe_rd=cr&ei=GaLvWNGjIOOv8wf2g634Dw%23q=major+tree+species+in+polish+forests&start=10https://www.google.pl/search?q=gatunki+drzewa+w+polsce&ie=utf-8&oe=utf-8&client=firefox-b&gfe_rd=cr&ei=GaLvWNGjIOOv8wf2g634Dw%23q=major+tree+species+in+polish+forests&start=10http://www.sciencep.com

Analysis of some metallic elements and metalloids composition and relationships in parasol mushroom Macrolepiota proceraAbstractIntroductionMaterials and methodsResults and discussionToxic metallic elements and metalloidsMultivariate analysis of data

ConclusionReferences